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Published in: Brain Structure and Function 7/2021

Open Access 01-09-2021 | Original Article

Transmitter and ion channel profiles of neurons in the primate abducens and trochlear nuclei

Authors: Ümit Suat Mayadali, Jérome Fleuriet, Michael Mustari, Hans Straka, Anja Kerstin Ellen Horn

Published in: Brain Structure and Function | Issue 7/2021

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Abstract

Extraocular motoneurons initiate dynamically different eye movements, including saccades, smooth pursuit and vestibulo-ocular reflexes. These motoneurons subdivide into two main types based on the structure of the neuro-muscular interface: motoneurons of singly-innervated (SIF), and motoneurons of multiply-innervated muscle fibers (MIF). SIF motoneurons are thought to provoke strong and brief/fast muscle contractions, whereas MIF motoneurons initiate prolonged, slow contractions. While relevant for adequate functionality, transmitter and ion channel profiles associated with the morpho-physiological differences between these motoneuron types, have not been elucidated so far. This prompted us to investigate the expression of voltage-gated potassium, sodium and calcium ion channels (Kv1.1, Kv3.1b, Nav1.6, Cav3.13.3, KCC2), the transmitter profiles of their presynaptic terminals (vGlut1 and 2, GlyT2 and GAD) and transmitter receptors (GluR2/3, NMDAR1, GlyR1α) using immunohistochemical analyses of abducens and trochlear motoneurons and of abducens internuclear neurons (INTs) in macaque monkeys. The main findings were: (1) MIF and SIF motoneurons express unique voltage-gated ion channel profiles, respectively, likely accounting for differences in intrinsic membrane properties. (2) Presynaptic glutamatergic synapses utilize vGlut2, but not vGlut1. (3) Trochlear motoneurons receive GABAergic inputs, abducens neurons receive both GABAergic and glycinergic inputs. (4) Synaptic densities differ between MIF and SIF motoneurons, with MIF motoneurons receiving fewer terminals. (5) Glutamatergic receptor subtypes differ between MIF and SIF motoneurons. While NMDAR1 is intensely expressed in INTs, MIF motoneurons lack this receptor subtype entirely. The obtained cell-type-specific transmitter and conductance profiles illuminate the structural substrates responsible for differential contributions of neurons in the abducens and trochlear nuclei to eye movements.
Literature
go back to reference Büttner-Ennever JA (1992) Paramedian tract cell groups: a review of connectivity and oculomotor function. In: Shimazu H, Shinoda Y (eds) Vestibular and brain stem control of eye, head and body movements. Japan Scientific Societies Press, Karger, Tokyo, Basel, pp 323–330. https://doi.org/10.1159/000421392CrossRef Büttner-Ennever JA (1992) Paramedian tract cell groups: a review of connectivity and oculomotor function. In: Shimazu H, Shinoda Y (eds) Vestibular and brain stem control of eye, head and body movements. Japan Scientific Societies Press, Karger, Tokyo, Basel, pp 323–330. https://​doi.​org/​10.​1159/​000421392CrossRef
go back to reference Delgado-García JM, Baker R, Highstein S (1977) The activity of internuclear neurons identified within the abducens nucleus of the alert cat. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 291–300 Delgado-García JM, Baker R, Highstein S (1977) The activity of internuclear neurons identified within the abducens nucleus of the alert cat. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 291–300
go back to reference Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61PubMed Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61PubMed
go back to reference Highstein SM, Karabelas A, Baker R, McCrea RA (1982) Comparison of the morphology of physiologically identified abducens motor and internuclear neurons in the cat: a light microscopic study employing the intracellular injection of horseradish peroxidase. J Comp Neurol 208:369–381. https://doi.org/10.1002/cne.902080407CrossRefPubMed Highstein SM, Karabelas A, Baker R, McCrea RA (1982) Comparison of the morphology of physiologically identified abducens motor and internuclear neurons in the cat: a light microscopic study employing the intracellular injection of horseradish peroxidase. J Comp Neurol 208:369–381. https://​doi.​org/​10.​1002/​cne.​902080407CrossRefPubMed
go back to reference Leigh RJ, Zee DS (2015) The neurology of eye movements. Oxford University Press, OxfordCrossRef Leigh RJ, Zee DS (2015) The neurology of eye movements. Oxford University Press, OxfordCrossRef
go back to reference McElligott J, Spencer R (2000) Neuropharmacological aspects of the vestibulo-ocular reflex. In: Beitz AJ, Anderson JH (eds) Neurochemistry of the vestibular system, vol 10. CRC Press, Boca Raton, pp 199–222 McElligott J, Spencer R (2000) Neuropharmacological aspects of the vestibulo-ocular reflex. In: Beitz AJ, Anderson JH (eds) Neurochemistry of the vestibular system, vol 10. CRC Press, Boca Raton, pp 199–222
go back to reference Ugolini G, Klam F, Doldan Dans M, Dubayle D, Brandi A-M, Büttner-Ennever JA, Graf W (2006) Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to “slow” and “fast” abducens motoneurons. J Comp Neurol 498:762–785. https://doi.org/10.1002/cne.21092CrossRefPubMed Ugolini G, Klam F, Doldan Dans M, Dubayle D, Brandi A-M, Büttner-Ennever JA, Graf W (2006) Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to “slow” and “fast” abducens motoneurons. J Comp Neurol 498:762–785. https://​doi.​org/​10.​1002/​cne.​21092CrossRefPubMed
Metadata
Title
Transmitter and ion channel profiles of neurons in the primate abducens and trochlear nuclei
Authors
Ümit Suat Mayadali
Jérome Fleuriet
Michael Mustari
Hans Straka
Anja Kerstin Ellen Horn
Publication date
01-09-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02315-7

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